Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin

According to life-history theory, long-lived birds should favor their survival over the current reproductive attempt, when breeding becomes too costly. In seabirds, incubation is often associated with spontaneous long-term fasting. Below a threshold in body reserves, hormonal and metabolic shift characteristics of a switch from lipid to protein utilization (phase III, PIII) occur. These metabolic changes are paralleled by nest abandonment and stimulation of refeeding behavior. Parental behavior is then under control of two hormones with opposite effects: corticosterone (CORT) and prolactin which stimulate foraging and incubation behavior, respectively.The aim of this study was to determine the respective role of these two hormones in nest abandonment by Adélie penguins. To this end, plasma hormone levels were measured before egg-laying and at departure from the colony (i.e. when birds were relieved by their partner or abandoned their nest), and related to nutritional state and incubation success.We found that males abandoning their nest in PIII presented high CORT levels and low prolactin levels. Interestingly, males which presented high plasma levels of prolactin in PIII did not abandon. We show that although CORT is the first hormone to be affected by prolonged energy constraints, the combined effects of high CORT and low prolactin levels are necessary for parents to favor self-maintenance and abandon the nest. We provide insights into time-course changes of the endocrine profile as PIII proceeds and report that reaching proteolytic late fasting is not sufficient to induce nest abandonment in a long-lived bird.     

Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird,the Adélie penguin

According to life-history theory, long-lived birds should favor their survival over the current reproductive attempt, when breeding becomes too costly. In seabirds, incubation is often associated with spontaneous long-term fasting. Below a threshold in body reserves, hormonal and metabolic shift characteristics of a switch from lipid to protein utilization (phase III, PIII) occur. These metabolic changes are paralleled by nest abandonment and stimulation of refeeding behavior. Parental behavior is then under control of two hormones with opposite effects: corticosterone (CORT) and prolactin which stimulate foraging and incubation behavior, respectively.The aim of this study was to determine the respective role of these two hormones in nest abandonment by Adélie penguins. To this end, plasma hormone levels were measured before egg-laying and at departure from the colony (i.e. when birds were relieved by their partner or abandoned their nest), and related to nutritional state and incubation success.We found that males abandoning their nest in PIII presented high CORT levels and low prolactin levels. Interestingly, males which presented high plasma levels of prolactin in PIII did not abandon. We show that although CORT is the first hormone to be affected by prolonged energy constraints, the combined effects of high CORT and low prolactin levels are necessary for parents to favor self-maintenance and abandon the nest. We provide insights into time-course changes of the endocrine profile as PIII proceeds and report that reaching proteolytic late fasting is not sufficient to induce nest abandonment in a long-lived bird.     

Human-induced behaviour in Adélie penguins Pygoscelis adeliae

Summary Adélie penguins Pygoscelis adeliae appear to be little perturbed by man. We examined the incidence of nest desertion and duration of foraging trip in Adélie penguins when manipulated and fitted with devices of differing sizes. Birds with ca. 1 cm clipped from their tail feathers stayed at sea 50% longer than unmarked controls. The length of foraging trip and incidence of nest desertion increased with increasing device volume. Penguins fitted with devices did not reduce foraging trip length to that of unpackaged birds for at least 19 days. The susceptibility of Adélie penguins to disturbance should be carefully considered when activity patterns are being studied.     

Exogenous corticosterone mimics a late fasting stage in captive Adelie penguins (Pygoscelis adeliae)

Fasting is part of penguin's breeding constraints. During prolonged fasting, three metabolic phases occur successively. Below a threshold in body reserves, birds enter phase III (PIII), which is characterized by hormonal and metabolic shifts. These changes are concomitant with egg abandonment in the wild and increased locomotor activity in captivity. Because corticosterone (CORT) enhances foraging activity, we investigated the variations of endogenous CORT, and the effects of exogenous CORT on the behavioral, hormonal, and metabolic responses of failed breeder Adélie penguins. Untreated and treated captive male birds were regularly weighed and sampled for blood while fasting, and locomotor activity was recorded daily. Treated birds were implanted with various doses of CORT during phase II. Untreated penguins entering PIII had increased CORT (3.5-fold) and uric acid (4-fold; reflecting protein catabolism) levels, concomitantly with a rise in locomotor activity (2-fold), while prolactin (involved in parental care in birds) levels declined by 33%. In CORT-treated birds, an inverted-U relationship was obtained between CORT levels and locomotor activity. The greatest increase in locomotor activity was observed in birds implanted with a high dose of CORT (C100), locomotor activity showing a 2.5-fold increase, 4 days after implantation to a level similar to that of birds in PIII. Moreover, uric acid levels increased three-fold in C100-birds, while prolactin levels declined by 30%. The experimentally induced rise in CORT levels mimicked metabolic, hormonal, and behavioral changes, characterizing late fasting, thus supporting a role for this hormone in the enhanced drive for refeeding occurring in long-term fasting birds.     

Delayed laying and prolonged fasting in Adélie Penguins Pygoscelis adeliae

Observations of nesting Adélie Penguins (Pygoscelis adeliae) were made at Ardley Island during spring 1990 when snow cover was unusually thick at some subcolony sites. Adélie Penguins at these sites had to delay egg laying until the snow melted. Maximum length of fasting periods comprising pre-breeding and incubation was 50 days. Long fasting seemed to have no detrimental effect on breeding. Furthermore, there was no relationship between penguin arrival mass and duration of fast. Even birds with small mass had sufficient reserves to undergo long fasting periods.In spring 1990, when we started with a monitoring study for CEMP (CCAMLR 1990) at Ardley Island, there were still high quantities of snow at the subcolony sites. Adélie Penguins at Ardley Island inhabit both small rocky outcrops and flat, stony hillocks (storm bars). The latter had a distinctly thicker snow cover at this time so that the pebbles necessary for nest building were unattainable. Consequently, we observed the behaviour of the penguins in this situation, recorded the laying dates and lengths of fasting periods.     

Spontaneous egg or chick abandonment in energy-depleted king penguins: a role for corticosterone and prolactin?

Various exogenous or endogenous factors may induce an emergency response in birds, redirecting current activity towards survival. In fasting, breeding penguins, the achievement of a critical energy depletion was suggested to induce egg abandonment and departure to sea for re-feeding. How such a behavioral shift is hormonally controlled remains unknown. The possible involvement of corticosterone and prolactin was examined by characterizing the nutritional and hormonal states of king penguins at egg abandonment. Further, we tested if these states differ according to whether an egg or a chick is abandoned, and according to the timing of breeding. In every case of abandonment, birds were in phase III fasting characterized by accelerated protein catabolism. However, body condition at egg abandonment was lower in early than in late breeders, suggesting that king penguins are willing to tolerate a larger energy depletion when their potential breeding success is high. At egg and chick abandonment, plasma corticosterone levels were, respectively, increased by 2- and 4-fold, whereas plasma prolactin levels were, respectively, depressed by 3- and 1.4-fold. The increase in plasma corticosterone and the decrease in plasma prolactin could be involved in the control of abandonment by, respectively, stimulating the drive to re-feed and diminishing the drive to incubate or brood. The smaller decrease in prolactin levels and the greater increase in corticosterone levels observed at chick vs egg abandonment suggest that, in addition to nutritionally-related stimuli, tactile or audible stimuli from the egg or chick could intervene in the endocrine control of abandonment.     

Field metabolic rates of instrumented Adélie penguins using double-labelled water

Summary Adélie penguins (Pygoscelis adeliae) carrying dummy instruments were used to determine field metabolic rates using double-labelled water. All penguins injected with double-labelled water showed a marked loss of body mass (-4.5%) during the period of the experiments (20–131 h), irrespective of the time of the breeding season. Total body water averaged 57.3% and water flux estimates of field metabolic rates correlated with double-labelled water estimates of field metabolic rate (r ²=0.68), indicating that Adélie penguins do not ingest significant amounts of sea water. Brooding Adélie penguins had a mean field metabolic rate of 10.1 W·kg^-1 and at sea a field metabolic rate of 13.3 W·kg^-1, both of which compare well with previously published estimates based on time/activity budgets and respirometry. Mean field metabolic rate in penguins with crèching chicks was 14.1 W·kg^-1, and the birds spent 65 h absent from the nest as opposed to previous estimates of 7.1 W·kg^-1 and 21 h. The effects of weather, disturbance and manipulation on the behaviour and field metabolic rate of penguins late in the breeding season are discussed. Adélie penguins (crèching chicks) equipped with externally attached instruments spent more time absent from the nest than noninstrumented controls (76 vs 54 h), but had a lower field metabolic rate.Abbreviations ANOVA analysis of variance - DLW double-labelled water - FMR field metabolic rate - MR metabolic rate - RMR resting metabolic rate - TBW total body water - VSMOW Vienna standard mean ocean water - WF water flux     

People in Antarctica — how much do Adélie Penguins Pygoscelis adeliae care?

Summary In the course of physiological field studies, we opportunistically examined the effects of humans and aircraft on breeding Adélie Penguins Pygoscelis adeliae. Proximity to both aircraft and humans caused substantial increases in penguin heart rate even when no external stress was manifest. A solitary human at 20 m distance from commuting penguins on a well-used pathway caused the birds to deviate by 70 m. Birds at nests exposed to a single human fled much more readily when the brood consisted of large chicks (critical distance 6.1 m) rather than small chicks (critical distance 1.3 m) or eggs (critical distance 0.3 m). Aircraft caused birds to panic at distances greater than 1,000 m and 3 days exposure to a helicopter inhibited birds that had been foraging from returning to their nests, caused bird numbers in the colonies to decrease by 15% and produced an active nest mortality of 8%. Based on this data, we make recommendations to minimize stress on Adélie Penguin colonies exposed to man.     

Satellite tracking of Adélie penguins

Summary Female Adélie penguins (Pygoscelis adeliae) that take too long on their first post-laying foraging trip are a major cause of breeding failure, but in the ice-filled waters of Antarctica, determining where they go and why they are away so long has proved difficult. Here we describe the first successful attempt to track penguins at sea using satellite telemetry. Four females foraged in different locations, dispelling the notion of a common feeding ground. They moved up to 272 km from the rookery and covered from 551 to 1,121 km on their trips, swimming at minimum average speeds around 1.2 m/s. The birds were most likely to be in the water between 0630 and 1430 when light intensity, important for a visual predator, was greatest. Carrying the transmitters reduced rates of fat deposition (weight gain), increasing the duration of foraging trips of females, and suggested that they may forage until their fat depots reach a minimum threshold level. This has two implications: (i) durations of these postlaying foraging trips could potentially be used as an indicator of krill abundance (Euphausia sp), the almost exclusive food of Adélie penguins during this period, and (ii) any reduction in krill stocks caused by harvesting could increase foraging trip durations with a concomitant increase mi breeding failures.     

Restoration of body mass in King Penguins after egg abandonment at a critical energy depletion stage: early vs late breeders

In fasting‐incubating seabirds, it has been proposed that egg abandonment and refeeding should be induced when a low body mass (BM) threshold is attained, thus ensuring adult survival at the expense of immediate breeding. In the context of life‐history trade‐offs in long‐lived birds, we have tested this hypothesis by comparing short‐term survival and restoration of BM in King Penguins Aptenodytes patagonicus that abandoned their egg to those that were relieved normally by their mate at the end of the first incubation shift. Since King Penguins have an extended laying period, the possible influence of seasonal factors was also examined by comparing early and late breeders. Forty incubating males were experimentally forced to fast until egg abandonment by preventing relief by the female. At egg abandonment of both early and late breeding males, BM was below the BM threshold, fasting duration was eight days (about 30%) longer than for relieved birds, and plasma uric acid level was elevated (signature of increased body protein catabolism, phase III of fasting). All abandoning birds survived and came back from sea at a BM similar to that of relieved penguins. The duration of the foraging trip of abandoning early breeders was the same as that of relieved birds, and some abandoning birds engaged in a new breeding attempt. Abandoning late breeders, however, made foraging trips twice as long as those of relieved males. This difference can be explained by time constraints rather than nutritional constraints, abandoning early breeders having enough time left in the breeding season to engage in a new breeding attempt in contrast to abandoning late breeders. These observations lend support to the suggestion that not only BM but also an internal clock intervene in the decision to engage in breeding or not. By preventing a lethal energy depletion ashore and by acting at a fasting stage where the capacity to restore BM at sea is unaffected, abandonment at a low body condition threshold plays a major role in the trade‐off between adult penguin survival and reproduction.     

Physiological condition and reproductive consequences in adelie penguins

Animals must make "decisions" (e.g., when or whether to breed,the effort to put into a breeding episode) by integrating physiological,environmental and social inputs. This integration can be studiedonly in a field context. In Adélie penguins (Pygoscelisadeliae) reproduction is constrained by foraging ecology, modeof transport, and the extreme latitude at which they live. Thedecision whether to breed in a given year is influenced by bodyconditions. Adélie penguins must fast for several weeksduring the early reproductive stages and use stored fat formetabolic energy. Females that return to the colony, but donot breed, are 10–12% lighter than females that do breed.Birds that are relatively low in body mass tend to have lowerreproductive success than heavier birds, and an individual'sreproductive success is positively correlated with the bodyfat stores it had on arrival. After eggs are laid, parents alternatein attending the nest. Nest failure occurs if one parent doesnot make a timely return and its fasting partner must eventuallyleave. During normal-length fasts plasma corticosterone andglucose levels do not change. Blood ß-hydroxybutyratelevels gradually increase during the fast while uric acid levelsremain low, but in birds with the longest fasts (>50 days),ketone levels may fall and uric acid levels increase, indicativeof a switch from using fat to using body proteins for metabolism.In incubating males, hematocrit and hemoglobin concentrationsalso increase, suggesting dehydration can accompany energy stressduring the breeding fast.     

Prolactin and parental behavior in Adélie penguins: effects of absence from nest, incubation length, and nest failure

Adélie penguin (Pygoscelis adeliae) males and females, nesting in Antarctica, alternate attendance at the nest with absences of many days to forage at sea. We investigated the importance of tactile input from egg and chicks on prolactin levels by observing nest attendance patterns and obtaining blood samples (1) during the first nest exchange of the incubation stage, (2) from birds whose incubation period was artificially increased or decreased by about 10 days, and (3) from birds whose nests had failed. Prolactin levels in females after 8 to 11 days of absence from the breeding colony did not differ from those in incubating males and did not change after females resumed incubation. Moving eggs between nests resulted in nests in which chicks hatched after about 26, 36 (normal), or 46 days. Duration of incubation did not affect prolactin levels in the parents measured during incubation, at the pip stage, hatch stage, or early brood stage. Adults first left their chicks unguarded on about the same calendar date, regardless of chick age. However, chicks from long incubation nests averaged 8 days younger when they were left unguarded than chicks from control or short-incubation nests. In females, there was no effect of nest failure on prolactin levels. In males, prolactin levels were slightly lower after nest failure than in males tending nests. Testosterone was significantly higher in males after nest failure than in males still tending nests. Prolactin is elevated in Adélie penguins as part of the program of cyclical hormonal changes that accompany the lengthy reproductive season and is relatively independent of tactile input. Sustained prolactin secretion is probably required for the maintenance of parental behavior in offshore feeding species that must be absent from the nest for many days at a time.     

Refeeding signal in fasting-incubating king penguins: changes in behavior and egg temperature

This study is directed toward understanding the process of feeding stimulation ("refeeding signal") that has been suggested to operate below a body mass threshold or critical metabolic status in spontaneously fasting birds. Behavior and egg temperature (T(egg)) were continuously monitored by video monitoring and biotelemetry, respectively, in fasting-incubating king penguins kept in a pen to prevent relief by the partner until spontaneous egg abandonment. Penned birds fasted 10 days more and lost 1.2 kg more than birds relieved normally by their partner, abandoning the egg about 1 wk after reaching a critical body mass. Definitive egg abandonment was preceded by transitory abandonments of progressively increasing duration during which time the birds went further and further away from their egg. There were marked interindividual differences but on average transitory abandonments began 36 +/- 5 h before the definitive abandonment and were paralleled by resumption of display songs signaling the readiness of the bird to depart for feeding. T(egg) was maintained at around 35.7 degrees C during normal incubation but significantly decreased the last 2 days before egg abandonment. These changes are interpreted as reflecting a stimulation to refeed at a threshold body mass corresponding to a critical fat store depletion. Thus the fasting-incubating king penguin appears to be an interesting animal model for understanding the long-term metabolic control of feeding behavior in relation to energy status.     

Mediation of a corticosterone-induced reproductive conflict

Current research in birds suggests that a conflict should exist during reproduction for the role of the glucocorticoid corticosterone (CORT). While elevated levels have been correlated with the increased energetic demand of raising offspring, elevated CORT levels have traditionally been implicated in reproductive abandonment. We examined the relationship between CORT and nest desertion in breeding wild female European starlings (Sturnus vulgaris) incorporating analyses of both total circulating levels and 'free', unbound CORT through analysis of corticosteroid-binding globulin (CBG). Free baseline CORT levels of nest-abandoning birds were significantly higher than nonabandoning birds within each stage, with chick-rearing birds exhibiting the highest free baseline CORT levels, while concurrently remaining the most resistant stage to nest desertion. Elevated free baseline CORT levels in chick-rearing birds were not due to increased total CORT secretion, but rather to a decrease in CBG levels. Overall, our results suggest that CORT and CBG interact to play a role in mediating the increased energetic demand of offspring, while minimizing the chances of nest desertion, thereby alleviating any potential behavioral conflict for CORT during reproduction. Furthermore, these results demonstrate that the traditional view of the role of CORT during reproduction is much more complex than previously appreciated. Together with mounting evidence, we suggest that elevated corticosteroid levels are an inherent and necessary part of reproduction in nonmammalian tetrapods.     

Energetic costs of raising Pygoscelid penguin chicks

Energy requirements of resting Adélie (Pygoscelis adeliae), Gentoo (P. papua) and Chinstrap (P. antarcticd) penguin chicks were determined with respect to body mass via respirometry in Antarctica. Resting metabolic rates of all Pygoscelid penguin chicks were similar (ANOVA p=0.91) and best described by E=0.0096 M^0.98 (n=24, r²=0.97), where E is power (W) and M is mass (g). Using the results obtained here and data published in the literature, I determined a) the amount of food needed from hatching to fledging as 29.8, 31.7 and 56.4 kg per chick for Adélie, Chinstrap and Gentoo penguins, respectively and b) the average amount of food left daily to the parent after feeding the brood throughout the breeding period. Parents keep only a minimum of food for themselves just prior to the time when chicks begin forming crèches. Thereafter, nest relief intervals are increased, and the amount of food parents can keep for themselves rises. The results of both models are discussed with respect to available data on Pygoscelid penguin food requirements.     

Endocrine correlates of parental care in an Antarctic winter breeding seabird, the emperor penguin, Aptenodytes forsteri

Plasma levels of luteinizing hormone (LH) and prolactin associated with parental behavior were measured in the Antarctic winter breeding emperor penguin, Aptenodytes forsteri. Males exclusively incubate the egg while females exclusively brood the nonhomeothermic young; both sexes alternate in rearing the homeothermic young. Birds were sampled on arrival from the sea through egg laying, incubation, and brooding. All parent birds lost their chicks at the end of the brooding period due to harsh weather but sampling continued. In females, LH titers dropped after egg laying but levels were restored when the birds returned from the sea to brood the chicks and were not depressed by high prolactin levels. Plasma prolactin remained low in males captured on arrival and kept until the free-living males finished incubation. In breeders, prolactin secretion increased during the prelaying period when day length decreased. Prolactin levels stayed elevated in males during incubation and in brooding females returning after a 2-month absence at sea. Prolactin values were higher in brooding females than in males ending incubation or returning in late brooding. These levels did not drop after chick loss, and the sexual difference in prolactin values was maintained after breeding failure. In emperor penguins, increased prolactin secretion appears to be triggered around the time of egg laying and continues, driven by an endogenous mechanism, through incubation and brooding until rearing is completed. Prolactin secretion independent of external stimuli may have evolved in pelagic seabirds to maintain parental care despite long absences at sea from the breeding colony.     

Pygoscelid penguins in a swim canal

Summary In Antarctica, we investigated the energy consumption of Adélie (Pygoscelis adeliae), Gentoo (P. papua) and Chinstrap (P. antarctica) penguins while resting in the water (8.4 W-kg^–1) and swimming underwater at various speeds, using a 21m long canal filled with sea-water at 4°C in conjunction with respirometry. The birds swam at will and consumed 15.7, 16.1 and 10 W·kg^–1 at the speed where cost of transport was minimal (2.1, 2.3 and 2.5 m·s^–1 in Adélie, Gentoo and Chinstrap penguins, respectively). Thermal conductance in pygoscelid penguins was 3.3 W·°C^–1. m^–2 and energy expenditure (P_i, W·kg^–1) while resting in the water is given by P_j = -0.3 t_a+9.6, where t_a is water temperature in °C. During the breeding season, pygoscelid penguins spend 25–40% of their daily energy expenditure while foraging at sea. The importance of accurate estimates of at-sea activity and energy consumption is discussed.     

Diet and reproductive success of Adélie and chinstrap penguins: linking response of predators to prey population dynamics

The diet and reproductive performance of two sympatric penguin species were studied at Signy Island, South Orkney Islands between 1997 and 2001. Each year, Adélie (Pygoscelis adeliae) and chinstrap (P. antarctica) penguins fed almost exclusively (>99% by mass) on Antarctic krill; however, there was considerable inter-annual variation in reproductive output. In 1998, chinstrap penguins were adversely affected by extensive sea-ice in the vicinity of the colony, whereas Adélie penguins were unaffected by this. However, in 2000, both species suffered reduced reproductive output. Detailed analysis of the population-size structure of krill in the diet indicated a lack of recruitment of small krill into the population since 1996. A simple model of krill growth and mortality indicated that the biomass represented by the last recruiting cohort would decline dramatically between 1999 and 2000. Thus, despite the lack of a change in the proportion of krill in the diet, the population demographics of the krill population suggested that the abundance of krill may have fallen below the level required to support normal breeding success of penguins sometime before or during the 2000 breeding season. The role of marine predators as indicator species is greatly enhanced when studies provide data reflecting not only the consequences of changes in the ecosystem but also those data that elucidate the causes of such changes.     

Euphausia superba dominates in the diet of Adélie penguins feeding under fast sea-ice in the shelf areas of Enderby Land in summer

Adélie penguins Pygoscelis adeliae in Enderby Land, Antarctica feed mainly on Euphausia superba during the chick rearing season in shelf areas where fast sea-ice remains: indicating that E. superba is abundant under the fast sea-ice in these areas. The shelf areas in Enderby Land, therefore, are unique since the previous studies of Adélie penguin diet in Ross Sea, Adélie Land and Prydz Bay show that E. crystallorophias is the most abundant krill species in shelf areas in general.     

Body mass and clutch size may modulate prolactin and corticosterone levels in eiders

Altered body condition, increased incubation costs, and egg loss are important proximate factors modulating bird parental behavior, since they inform the adult about its remaining chances of survival or about the expected current reproductive success. Hormonal changes should reflect internal or external stimuli, since corticosterone levels (inducing nest abandonment) are known to increase while body condition deteriorates, and prolactin levels (stimulating incubation) decrease following egg predation. However, in a capital incubator that based its investment on available body reserves and naturally lost about half of its body mass during incubation, corticosterone should be maintained at a low threshold to avoid protein mobilization for energy supply. This study focused on the regulation of corticosterone and prolactin release in such birds during incubation, when facing egg manipulation (control, reduced, or increased) or a stressful event. Blood samples were taken before and after clutch manipulation and at hatching. Corticosterone levels were determined before and after 30 min of captivity. Female eiders exhibited a high hypothalamic-pituitary-adrenal sensitivity, plasma concentration of corticosterone being increased by four- to fivefold following 30 min of captivity. The adrenocortical response was not modified by body mass loss but was higher in birds for which clutch size was increased. In the same way, females did not show different prolactin levels among the experimental groups. However, when incubation started, prolactin levels were correlated to body mass, suggesting that nest attendance is programmed in relation to the female initial body condition. Moreover, due to an artifactual impact of bird manipulation, increased baseline corticosterone was associated with a prolactin decrease in the control group. These data suggest that, in eiders, body mass and clutch size modification can modulate prolactin and corticosterone levels, which cross-regulate each other in order to finely control incubation behavior.